Primary IMHA in dogs is characterized by RBC destruction and is associated with a high mortality rate. A prothrombotic state and subsequent thromboembolic disease is thought to be a major contributor to death of dogs with this disease.1–3 Most dogs with idiopathic IMHA are in a hypercoagulable state at the time of diagnosis, and it is likely that hemolysis is an important instigating factor.2 Several mechanisms have been proposed to cause a hypercoagulable state in IMHA, with the most likely sources being a combination of alterations in cytokine release, number of activated platelets, and concentrations of tissue factor, antithrombin III, fibrinogen, soluble fibrin, and D-dimers.1,2
According to Poiseuille's law, resistance to blood flow is proportional to vessel length and blood viscosity. The decrease in blood viscosity with hemolytic anemia is expected to contribute to a decreased resistance in flow. Experimentally induced normovolemic anemia results in significant increases in PV blood flow in dogs,4 which is similar to results of a study5 performed with an anemic newborn lamb. It is postulated that the complex interactions of an altered hemodynamic state, activated endothelium, and reduced viscosity in dogs with IMHA affect blood flow velocities in various unknown manners. Investigators of an in vitro study6 determined that as blood flow velocity near an endothelial surface increases, shear stress also increases, which results in an increasingly fibrinolytic state.
Standard diagnostic evaluations to determine the primary causes of IMHA include a complete abdominal ultrasonographic examination. Given that most cases of IMHA are primary, results of the abdominal ultrasonographic examination rarely alter the treatment plan or provide additional prognostic information; however, it can be used to exclude secondary causes such as neoplastic disease or severe infection. Pulsed-wave Doppler imaging has been used primarily to evaluate the PV of dogs during the assessment of portosystemic shunts and portal hypertension; mean blood flow velocities of the PV have been reported.7 To our knowledge, quantitative assessment of blood flow velocities in the CVC of the cranial portion of the abdomen in clinically normal or diseased dogs has not been reported; however, there have been qualitative descriptions (a multiphasic waveform as a result of pressure changes in the right atrium), similar to descriptions reported for the hepatic veins of anesthetized dogs.8–12 Measurement of blood flow velocities in these main abdominal veins by use of pulsed-wave Doppler ultrasonography might expand the clinical use of abdominal ultrasonography for differentiating hypercoagulable dogs from clinically normal dogs.
The purpose of the study reported here was to compare peak blood flow velocity in the PV and CVC of clinically normal dogs and dogs with IMHA. We also intended to provide initial reference values for CVC flow velocities in healthy dogs. We hypothesized that clinically affected dogs will have a higher peak blood flow velocity in the PV and CVC, compared with peak blood flow velocity in clinically normal dogs.
Supported by the Michigan Animal Health Fund. Funding sources did not have any involvement in the study design, data analysis and interpretation, or writing and publication of the manuscript.
The authors declare that there were no conflicts of interest.
Caudal vena cava
Immune-mediated hemolytic anemia
Hemostasis analyzer 5000, Haemonetics, Niles, Ill.
GE Logiq S8, GE Medical Systems, Milwaukee, Wis.
R, version 1.0.44, R Core Team, Auckland, New Zealand.
R package pROC, version 1.8, R Core Team, Auckland, New Zealand.
Excel, version 12.3.6, Microsoft Corp, Redmond, Wash.
1. Kidd L, Mackman N. Prothrombotic mechanisms and anticoagulant therapy in dogs with immune-mediated hemolytic anemia. J Vet Emerg Crit Care (San Antonio) 2013;23:3–13.
2. Scott-Moncrieff JC, Treadwell NG, McCullough SM, et al. Hemostatic abnormalities in dogs with primary immune-mediated hemolytic anemia. J Am Anim Hosp Assoc 2001;37:220–227.
3. Fenty RK, Delaforcade AM, Shaw SE, et al. Identification of hypercoagulability in dogs with primary immune-mediated hemolytic anemia by means of thromboelastography. J Am Vet Med Assoc 2011;238:463–467.
4. Koma LM, Spotswood TC, Kirberger RM, et al. Influence of normovolemic anemia on Doppler characteristics of the abdominal aorta and splanchnic vessels in Beagles. Am J Vet Res 2005;66:187–195.
5. Taylor GA, Hudak ML. Color Doppler ultrasound of changes in small vessel diameter and cerebral blood flow during acute anemia in the newborn lamb. Invest Radiol 1994;29:188–194.
7. Lamb CR, Mahoney PN. Comparison of three methods for calculating portal blood flow velocity in dogs using duplex-Doppler ultrasonography. Vet Radiol Ultrasound 1994;35:190–194.
8. Szatmári VI, Sótonyi P, Vörös K. Normal duplex Doppler waveforms of major abdominal blood vessels in dogs: a review. Vet Radiol Ultrasound 2001;42:93–107.
9. Smithenson BT, Mattoon JS, Bonagura JD, et al. Pulsed-wave Doppler ultrasonographic evaluation of hepatic veins during variable hemodynamic states in healthy anesthetized dogs. Am J Vet Res 2004;65:734–740.
10. Nelson NC, Drost WT, Lerche P, et al. Noninvasive estimation of central venous pressure in anesthetized dogs by measurement of hepatic venous blood flow velocity and abdominal venous diameter. Vet Radiol Ultrasound 2010;51:313–323.
11. Abu-Yousef MM. Normal and respiratory variations of the hepatic and portal venous duplex Doppler waveforms with simultaneous electrocardiographic correlation. J Ultrasound Med 1992;11:263–268.
12. Coulden RA, Lomas DJ, Farman P, et al. Doppler ultrasound of the hepatic veins: normal appearances. Clin Radiol 1992;45:223–227.
13. Koenigshof AM, Scott MA, Brown AJ. Effects of delayed anticoagulation and use of evacuated tubes on non-activated thrombelastography in dogs. Vet Clin Pathol 2012;41:63–70.
14. Koma LM, Kirberger RM, Scholtz L, et al. Influence of normovolemic anemia on Doppler-derived blood velocity ratios of abdominal splanchnic vessels in clinically normal dogs. Vet Radiol Ultrasound 2005;46:427–433.
16. Sherwood JM, Kaliviotis E, Dusting J, et al. Hematocrit, viscosity and velocity distributions of aggregating and non-aggregating blood in a bifurcating microchannel. Biomech Model Mechanobiol 2014;13:259–273.
17. Yeom E, Kang YJ, Lee SJ. Changes in velocity profile according to blood viscosity in a microchannel. Biomicrofluidics 2014;8:034110.
18. Chien S, Dellenback RJ, Usami S, et al. Blood volume, hemodynamic, and metabolic changes in hemorrhagic shock in normal and splenectomized dogs. Am J Physiol 1973;225:866–879.
21. Mischke R. Hemostatic disorders as a complication of autoimmune hemolytic anemia in dogs. Dtsch Tierarztl Wochenschr 1998;105:13–16.
22. Sinnott VB, Otto CM. Use of thromboelastography in dogs with immune-mediated hemolytic anemia: 39 cases (2000–2008). J Vet Emerg Crit Care (San Antonio) 2009;19:484–488.
23. Wiinberg B, Jensen AL, Johansson PI, et al. Thromboelastographic evaluation of hemostatic function in dogs with disseminated intravascular coagulation. J Vet Intern Med 2008;22:357–365.
24. Brooks AC, Guillaumin J, Cooper ES, et al. Effects of hematocrit and red blood cell-independent viscosity on canine thromboelastographic tracings. Transfusion 2014;54:727–734.
25. Smith SA, McMichael MA, Gilor S, et al. Correlation of hematocrit, platelet concentration, and plasma coagulation factors with results of thromboelastometry in canine whole blood samples. Am J Vet Res 2012;73:789–798.
27. Flint SK, Abrams-Ogg AC, Kruth SA, et al. Independent and combined effects of prednisone and acetylsalicylic acid on thromboelastography variables in healthy dogs. Am J Vet Res 2011;72:1325–1332.
28. Patrassi GM, Sartori MT, Livi U, et al. Impairment of fibrinolytic potential in long-term steroid treatment after heart transplantation. Transplantation 1997;64:1610–1614.
32. Moriyasu F, Ban N, Nishida O, et al. Clinical application of an ultrasonic duplex system in the quantitative measurement of portal blood flow. J Clin Ultrasound 1986;14:579–588.
33. Kim J, Kim S, Eom K. Pulsed-wave Doppler ultrasonographic evaluation of hepatic vein in dogs with tricuspid regurgitation. J Vet Sci 2017;18:73–79.